BIO-INSPIRATION FROM NATURALLY HEALING TISSUES
P. Fratzl 1, W. Wagermaier 1, R. Weinkamer 1, J.W.C. Dunlop 1 and M.J. Harrington 1 1 Max Planck Institute of Colloids & Interfaces, Department of Biomaterials, 14424 Potsdam,Germany – e-mail: matt.harrington@mpikg.mpg.de; wolfgang.wagermaier@mpikg.mpg.de; richard.weinkamer@mpikg.mpg.de; john.dunlop@mpikg.mpg.de; peter.fratzl@mpikg.mpg.de
ABSTRACT
In the course of evolution, load-bearing biological materials have generally not evolved towards perfection and maximum strength, but instead developed high defect tolerance and adaptability [1]. Adaption occurs at various levels, see figure 1. While evolution leads to adaptation of entire species, each individual has mechanisms which confer some self-repair properties even at smaller scales to cope with a variety of environmental challenges. Healing and regeneration occur at the level of organs, but many biological materials are damage-tolerant at the supra-molecular level or have (passive) self-repair properties.
Figure 1: Three levels of natural adaptation to environmental influences [1]. (a) Darwinian evolution acts on the species level to adapt to long-term challenges, such as habitat, food type or predators. (b) Remodeling, healing or regeneration operate at
the organ level within an individual organism. (c) Biological materials, such as bone, extracellular tissue or protein fibers are damage tolerant and often have self-repair
mechanisms that operate on the supra-molecular level.
The lecture discusses some aspects of self-repairing natural tissues on the levels (b) and (c), as outlined in figure 1. Repeated loading, such as side-winds in trees leads to adaptive growth of the plant to better withstand these loads. Similarly, training in
biological material individual organism species Functional
burden self-repairing materialsDamage tolerant, Remodeling Adaptive growth Healing Regeneration Evolution (adaptation of entire species) External stimuli Training (Over-)loading Organ failure Extreme habitats Variationsin food Predators
Environment
(a)
(b)
(c)
ICSHM2013_________________________________________________________________________________ 8humans not only leads to an increase in muscle mass but also of bone mass and architecture through a remodeling process. The interesting difference between adaptive growth in woody plants and bone remodeling lies in the fact that bone can not only be synthesized but also be resorbed by cells, while wood growth is only additive. This results in different adaptation strategies [2].
Bone remodeling is also a process by which damaged tissue is continuously replaced by newly synthesized material and, thus, an interesting case to inspire self-repairing artificial materials. Bone remodeling generally depends on a dense network of mechanosensitive cells, called osteocytes. This network is such that all mineralized tissue in bone is not further away from the next osteocyte canaliculum than about one micron, making the network an extremely effective transport system [3]. While bone continuously repairs damage through remodeling, it needs a more complicated process to heal after a fracture occurred. The healing process is a matter of intensive research and we will report new data showing that both natural [4] and scaffold-supported [5] healing requires a mechanical interaction between the growing tissue and its surrounding, which can be rationalized by in-vitro experiments [6]. This is also true for the rapid re-growth of the deer antler, which is another interesting case study for natural material regeneration [7].
While bone remodeling and healing are processes operating at the organ level (similarly to many kinds of wound healing in animals or plants), there are also intrinsic material properties which provide damage tolerance and self-repair. Examples are deformable interfaces connecting stiff protein or polysaccharide fibers or mineral platelets and capable of absorbing large deformations in tissues, such as tendons or plant cell walls [8]. In some cases, damage is fully recovered over a short [9] or a longer [10] period of time, thus providing some type of self-repair. In this context, we will briefly mention pseudo-elastic properties of whelk egg capsules [9] and a self-healing protein system in the mussel byssus [10].
Nature has evolved a wide range of mechanisms to cope with damage and imperfection in general. They exist as passive mechanisms within the material itself or they are controlled (at a much larger scale) by cells which add and/or remove material as needed. We are only beginning to unravel some of those principles. This lecture can only cover a very small selection of examples, based primarily on the authors’ own research interests.
REFERENCES
[1] R. Weinkamer, J.W.C. Dunlop, Y. Bréchet, P. Fratzl, All but diamonds: Biological materials are not forever, Acta Materialia 61 (2013) 880-889.
[2] R. Weinkamer, P. Fratzl, Mechanical adaptation of biological materials – The examples of bone and wood, Materials Science and Engineering C 31 (2011) 1164-1173.
[3] M. Kerschnitzki, P. Kollmannsberger, M. Burghammer, G.N. Duda, R. Weinkamer, W. Wagermaier, P. Fratzl, Architecture of the osteocyte network correlates with bone material quality, Journal of Bone and Mineral Research (2013) [Epub ahead of print] doi: 10.1002/jbmr.1927.
[4] M. Kerschnitzki, W. Wagermaier, Y. Liu, P. Roschger, G.N. Duda, P. Fratzl, Poorly Ordered Bone as an Endogenous Scaffold for the Deposition of Highly Oriented Lamellar Tissue in Rapidly Growing Ovine Bone, Cells Tissues Organs 194 (2011) 119-123.
[5] W.A. Woodruff, C. Lange, F. Chen, P. Fratzl, D.W. Hutmacher, Nano- to macroscale remodeling of functional tissue-engineered bone, Advanced Healthcare Materials 2 (2013) 546-551.
[6] C.M. Bidan, K.P. Kommareddy, M. Rumpler, P. Kollmannsberger, P. Fratzl, J.W.C. Dunlop, Geometry as a factor for tissue growth: towards shape optimization of tissue engineering scaffolds, Advanced Healthcare Materials 2 (2013) 186-194.
[7] S. Krauss, W. Wagermaier, J.A. Estevez, J.D. Currey, P. Fratzl, Tubular frameworks guiding orderly bone formation in the antler of the red deer (Cervus elaphus), Journal of Structural Biology 175 (2011) 457-464.
[8] J.W.C. Dunlop, R. Weinkamer, P. Fratzl, Artful interfaces within biological materials, Materials Today 3 (2011) 70-78.
[9] M.J. Harrington, S.S. Wasko, A. Masic, F.D. Fischer, H.S. Gupta, P. Fratzl, Pseudoelastic behaviour of a natural material is achieved via reversible changes in protein backbone conformation, Journal of the Royal Society Interface 9 (2012) 2911-2922.
[10] M.J. Harrington, H.S. Gupta, P. Fratzl, J.H. Waite, Collagen insulated from tensile damage by domains that unfold reversibly: In situ X-ray investigation of mechanical yield and damage repair in the mussel byssus, Journal of Structural Biology 167 (2009) 47-54.
